Latin American Journal of Aquatic Research, 48(1): 23-37, 2020 in a shallow lagoon-estuarine system

Fish assemblages 23
DOI: 10.3856/vol48-issue1-fulltext-2349

Research Article

The influence of habitat on the spatio-temporal dynamics of fish assemblages

in a lagoon-estuarine system of the Mexican Pacific

Emilio I. Romero-Berny1, Ernesto Velázquez-Velázquez2

Juan J. Schmitter-Soto3 & Isaías H. Salgado-Ugarte4
1
Centro de Investigaciones Costeras, Instituto de Ciencias Biológicas
Universidad de Ciencias y Artes de Chiapas, Tonalá, Chiapas, Mexico
2
Museo de Zoología, Instituto de Ciencias Biológicas
Universidad de Ciencias y Artes de Chiapas, Chiapas, Mexico
3
Departamento de Sistemática y Ecología Acuática, El Colegio de la Frontera Sur
Chetumal, Quintana Roo, Mexico
4
Laboratorio de Biometría y Biología Pesquera, Facultad de Estudios Superiores Zaragoza
Universidad Nacional Autónoma de México, Iztapalapa, Mexico City, Mexico
Corresponding author: Emilio I. Romero-Berny (emilio.romero@unicach.mx)

ABSTRACT. Fish assemblages change significantly with physical and chemical characteristics of water;
however, their response to the variability of geomorphic habitats has been rarely evaluated in lagoon-estuarine
in one of these systems of the Mexican Pacific. Spatio-temporal variation of fish assemblage structure was
assessed for three habitats: lagoon, estuarine, channel and inlet. The hypothesis was that sheltered areas support
comparatively higher richness and abundance of fish species, with more small-sized specimens than the most
exposed areas. We found that the ichthyofauna differed significantly among habitats. Several species were
smaller in the lagoon compared with the other habitats, suggesting a use of the lagoon as a nursery ground.
Moreover, dominant species for the lagoon were rarely found or absent in the inlet, whereas others were found
only present or with higher abundance in the inlet. Although seasonal differences in richness and composition
were detected, the evidence of fish-habitat associations for many species was noticeable regardless of
seasonality, probably due to a high percentage of resident species during the annual cycle. The lagoon supports
a greater abundance and species richness, due to a more sheltered and structured habitat, evidencing habitat-driven
segregation in fish assemblages, and an aspect that should be incorporated for management of coastal ecosystems.
Keywords: coastal; geoforms; habitat structure; ichthyofauna; nursery; Gulf of Tehuantepec

INTRODUCTION
Lagoon-estuarine systems are formed by a complex
matrix of intertidal habitats with distinctive environ-
mental features that play an essential role in support of
high fish production (McLusky & Elliott, 2004; Yáñez-
Arancibia et al., 2004; França et al., 2012). In these
systems, geomorphological processes originate geoforms
(e.g., lagoons, mouths and channels), which are habitats
with different physical attributes (e.g., depth, width,
substrate) that influence the patterns of composition,
richness, abundance, migration and the size-specific
spatial use by organisms (Bartholomew et al., 2000;
Saintilan, 2004; Franco et al., 2006; França et al., 2009;
Hicks et al., 2010). For example, the mouth and its tidal
channels are ecotones connecting the marine with the
brackish environment (Webster, 2011; Lacerda et al.,
2014). Furthermore, other geoforms such as lagoons,
which are partially enclosed areas with low water
circulation and more structural complexity (e.g., muddy
bottoms, riverine and submerged vegetation), are
reported as critical habitat for juvenile fish feeding and
nurseries (Neves et al., 2013; Verdiell-Cubedo et al.,
2013).
Habitat features have been integrated in estuarine
fish research as a key factor to understand the structure
of ecological assemblages and their relationship with
highly variable spatial conditions and allows to define

_________________
Corresponding editor: Yassir Torres
24 Latin American Journal of Aquatic Research

connectivity mechanisms between habitats and local compared to less complex areas, along spatial and
migration patterns (Sindilariu et al., 2006; Franco et al., seasonal gradients.
2009; Neves et al., 2011), as has been shown by several
studies carried out in estuaries and coastal lagoons of
MATERIALS AND METHODS
Europe, South Africa, Australia and South America
(Patterson & Whitfield, 2000; Griffiths, 2001; Franco
Study area
et al., 2006; Neves et al., 2011; Loureiro et al., 2016).
La Joya-Buenavista lagoon-estuarine system (LJB) is
Some studies have been conducted on fish assem-
located at the northeastern corner of Gulf of Tehuantepec,
blages of Mexican coasts, concerning mainly lagoon-
southwest Chiapas, Mexico (15°48’-15°56’N, 93°32’-
estuarine systems from the Gulf of Mexico and the
93°47’W); it is a shallow water body with an area of
northwest and central Pacific areas (Warburton, 1978;
47.5 km2 (Fig.1). The LJB presents a sandy barrier and
Mendoza et al., 2009; Castillo-Rivera et al., 2010;
tides predominantly semidiurnal, with a range of 1.2 m
Rodríguez-Romero et al., 2011; Ayala-Pérez et al.,
(Lankford, 1977; Contreras, 2010). The water circu-
2014). These studies indicate that physical and
lation into the system is reduced and depends mainly on
chemical changes (e.g., variations in salinity, water
the tides and the seasonal freshwater input provided by
temperature, turbidity, dissolved oxygen, etc.) asso-
a few streams. The climate in this area is characterized
ciated with seasonality constitute a significant driver of
by a dry season (November-April) and a rainy season
fish assemblage patterns. However, in the south Pacific
(May-October), with a total annual rainfall of 1,441
of Mexico there are no studies that include the effect of
mm and an average temperature of 28°C. The salinity
habitat complexity on fish assemblages.
can vary drastically in some areas, from oligohaline
The Gulf of Tehuantepec in the Mexican Southern (salinity <5) at the peak of the rains to hyperhaline
Pacific is one of the most important fishing areas (salinity >40) in highly protected sites during the dry
(Bakun et al., 1999; Ortega-García et al., 2000; season (Contreras & Zabalegui, 1991).
Wilkinson et al., 2009). This region has an extensive
belt of lagoon-estuarine systems surrounded by This study analyzed the fish assemblages of three
mangroves that shelters one of the richest areas for fish geomorphic habitats in the LJB system: lagoon,
fauna in the Tropical Mexican Pacific (Gómez- channel and inlet (Fig. 1). These habitats were
González et al., 2012; González-Acosta et al., 2017). identified mainly based on the qualitative description of
The environmental differences between the geomorphic physical and morphological characteristics. The depth
habitats that integrate these systems make them good of the lagoon varies from 0.2 to 1.5 m, with a
models to test the spatial effect of its characteristics on predominantly muddy substrate, with sparse submerged
biotic assemblages. tree trunks and margins comprised of grass and
The rapid degradation and loss of coastal
ecosystems in recent decades has increased interest in
fish research and their habitat in estuarine environments
(França et al., 2012; Sundblad & Bergström, 2014).
The knowledge of geomorphic habitats and their effect
on fish assemblages constitutes an important baseline
for the development of monitoring programs and
integrate ecosystem-based management of coastal
resources (Pérez-Ruzafa et al., 2007; Franco et al.,
2009; Sheaves et al., 2012). Therefore, the specific
aims of this study were to i) determine the spatio-
temporal variations of fish assemblages in a shallow
lagoon-estuarine system and compare its structure in
three geomorphic habitats (lagoon, channel, inlet); and
to ii) determine their relationships with hydrological
parameters (e.g., salinity, dissolved oxygen, depth) and
physical attributes (substrate, vegetation, shelter). The
tested hypothesis is that fish assemblages are likely to Figure 1. Map of the study area in the La Joya-Buenavista
differ among these habitats, with the most complex lagoon-estuarine system, Mexico. Symbols represent
areas supporting comparatively higher fish abundance, sampling sites coded by habitat type. Circles: lagoon,
richness and a higher number of small-sized organisms squares: channel, triangles: inlet.
 Fish assemblages in a shallow lagoon-estuarine system
fringe/basin mangroves (Avicennia germinans L. and
Conocarpus erectus L.). The channel has a total length
of 23 km and varies in width from about 570 m at the
mouth to 200 m at the head. Most of the channel zone
is surrounded by riverine mangroves (Rhizophora
mangle L.). Substrate composition changes from
muddy, with some sandy patches in the channel, to
predominantly sandy in the mouth. The inlet flows into
the Gulf of Tehuantepec through an estuary mouth of
157 m of width, the zone most exposed to tidal currents.
Data collection
Sampling was performed bimonthly from 9:00 to 16:00
h, at 13 sites during June 2013-April 2014. Sampling
was conducted using monofilament cast nets (4 m
diameter with 1.27 cm mesh). This gear could be used
in all sites under its temporal variations in depth and
habitat conditions, although an a priori characterization
focused on small and juvenile components was
assumed (Sheaves et al., 2007; Stein III et al., 2014).
The cast net was operated from the shoreline or a boat
by the same individual. Sampling effort was standardized
to 10 cast nets. This number of deployments was
determined by estimating the values of the asymptotes
of plot-based species accumulation curves for each
habitat in three pilot sites (R2 = 0.99, 0.94, 0.96). Cast
net deployments were done in a radius of up to 50 m,
thus avoiding the disturbance effect of three castings at
the same point.
The fish specimens were weighed, measured, fixed
in 10% formalin, washed in tap water after 48 h, and
transferred to 70% ethanol. All fish were identified to
species and counted. Scientific names and authorities
were corroborated following Fricke et al. (2019).
Voucher specimens were deposited at the ichthyo-
logical collection of the Museum of Zoology of the
University of Science and Arts of Chiapas (MZ-P-
UNICACH) in Tuxtla Gutiérrez, Mexico. For
descriptive purposes, selected dominant species were
allocated to four ecological categories according to
their salinity tolerance (Myers, 1966; Castro-Aguirre et
al., 1999; Day Jr. et al., 2012). These species were also
allocated to functional guilds according to their trophic
group following the criteria of Elliott et al. (2007), with
information from Froese & Pauly (2016). Four
ecological groups were identified in this study:
estuarine (fish that are residents in brackish waters),
marine euryhaline (can tolerate a wide range of
salinity), marine stenohaline (can tolerate a narrow
range of salinity) and secondary freshwater (salt-
tolerant inland fish). Likewise, five trophic groups were
identified: piscivores, which are species whose diet
consists mainly of fish; zooplanktivores, species that
feed predominantly on zooplankton; zoobenthivores,
25
species that feed on bottom invertebrates; detritivores,
species that feed on the bottom, selecting fine particles,
benthic diatoms, meiofauna and sediments; and
omnivores, which feed on algae and a variety of
invertebrates.
Hydrological variables were measured on each
sampling event before the fish collection. Salinity,
water temperature (°C), dissolved oxygen (mg L-1), and
pH were determined at the mid-depth of each site using
a multiprobe meter (YSI 556). The depth (to the nearest
0.1 m) and water clarity (Secchi´s depth in cm) were
also determined.
Habitat structure descriptors (substrate, vegetation
and shelter) were examined in the system (in this study,
habitat structure was considered as the physical
attributes that may provide protection and food for fish
species; Green et al., 2012). At each site, a plot of 1 m2
was randomly positioned to visually evaluate the
substrate composition as the percentage covered by
muddy, sandy or mixed deposits. The presence of other
physical elements as tree trunks and riprap was also
recorded. Values for vegetation were assigned based on
the dominant marginal coverage (>60% of mangroves
or grasses) in a 200 m2 area adjacent to the sampling
site. The shelter was assessed according to the distance
of the sites with the inlet or the channel. Following
Neves et al. (2013), each habitat attribute was assigned
a value from 1 to 3 to qualify structure, and these were
added to achieve a total score, estimated to obtain the
overall degree of physical habitat structure. Each site
was categorized with ranges from 3 (lowest habitat
structure) to 9 (highest habitat structure). For example,
highly exposed sites (such as the mouth) with bare sand
substrate and lacking plant (e.g., grasses) or physical
structures were qualified with a value of 3, whereas
other sites sheltered from the currents (such as the
lagoon), with a combination of muddy substrate,
submerged trunks and coverage dominated by mangroves
would get a score of 9.
Data analysis
The species dominance was determined using the
Importance Value Index (IV), estimated as a percentage
of the numerical abundance, biomass and frequency of
all species (Krebs, 1999). We considered species that,
in total, had 75% of the IV as dominant (Peralta-
Meixueiro & Vega-Cendejas, 2011).
The abundance data were fourth-root transformed to
minimize the influence of overly abundant taxa. The
data set was divided by the three geomorphic habitats
(lagoon, nine sites, inlet and channel, two sites each;
Fig. 1) and months were summarized in seasons as pre-
wet (June), wet (August-October), pre-dry (December)
and dry (February-April). An individual-based rarefac-
26 Latin American Journal of Aquatic Research
tion method was used to estimate the expected number
of species in a sample [E (Sn)] and calculate an
abundance-corrected dataset to compensate for diffe-
rences in sampling effort between habitats and seasons.
The E (S) was generated for a constant number in a
random set of m individuals from the reference sample
(m < n) (Colwell et al., 2012). The variation of the
rarefied species richness, as well as that of the
environmental parameters between habitat and season,
were analyzed using one-way analysis of variance
(ANOVA), having verified the assumptions of norma-
lity and homogeneity of variances. Non-parametric
ANOVA (Kruskal-Wallis test) was used in cases where
heteroscedasticity was found even after the logarithmic
transformation of data. A Bonferroni test (or Mann-
Whitney pairwise to non-parametric test) followed the
ANOVA procedures every time that the null hypothesis
was rejected at α = 0.05 (Zar, 2010).
Non-parametric multivariate analyses were
conducted to assess the spatio-temporal changes in fish
assemblage structure (species composition and
abundance) and their relationship to environmental
parameters, after evaluating the homogeneity of the
multivariate dispersion (PERMDISP) (Anderson, 2006).
Preliminarily, a permutational multivariate analysis of
variance (PERMANOVA) (Anderson, 2001), conducted
on a Euclidean similarity matrix of all environmental
data, assessed differences, and the interaction between
habitats and seasons. Furthermore, principal compo-
nent analysis (PCA) was performed on the normalized
hydrological data (log x+10) to explore gradients in the
sampling events. To avoid bias in the PCA related to
highly correlated hydrological data, before PCA, a
Pearson correlation test was performed, and variables
that show high collinearity (r > 8) were not considered
in this analysis. Later, differences in fish assemblages
between habitat and seasons were also assessed by
PERMANOVA, including habitat type (fixed factor),
seasons (fixed factor), sampling sites (nested in habitat
type) and months (nested in seasons), conducted on a
Bray-Curtis similarity matrix. A pairwise post-hoc
comparison was performed, while results off that
PERMANOVA were significant.
The similarity percentage analysis (SIMPER)
(Clarke, 1993) was used to describe the variance
explained per species by habitat. Standard length (SL)
data of dominant species selected by SIMPER were
compared with a Kruskal-Wallis test and the Mann-
Whitney pairwise test to assess possible variations in
the size of individuals per habitat.
Finally, distance-based linear modelling (DistLM)
(Anderson et al., 2008) with a step-wise procedure and
an adjusted R2 selection criterion (Legendre &
Anderson, 1999), was performed on the fourth-root
abundance matrix and the normalized environmental
data (including habitat structure values). The resulting
model was represented in a multi-dimensional space
with a distance-based redundancy analysis (dbRDA)
(McArdle & Anderson, 2001), to assess the relative
contributions of environmental variables in structuring
fish assemblage and detect a possible spatial gradient.
We worked with a 5% significance level (P ≤ 0.05) in
all statistical tests. All multivariate analyses were
performed with routines in PERMANOVA+ for
PRIMER 6 software (Clarke & Gorley, 2006; Anderson
et al., 2008). All other analyses were carried out with
package Vegan in language R, version 3.1.2 (Oksanen
et al., 2014; R Development Core Team, 2014).
RESULTS
Environmental variation
The PERMANOVA results showed that hydrological
variables were significantly different between habitats
(F = 9.25, P < 0.01), seasons (F = 18.98, P < 0.01) and
the interaction (habitat × season, F = 4.69, P < 0.01).
Likewise, differences in some hydrological parameters
were consistent (P < 0.05) between seasons and
habitats, or both. In paired comparisons within
temporal factor, major differences between habitats
were observed in all seasons (P < 0.02), except for the
inlet-channel pair; oxygen saturation was low during
the dry season in the channel (1 mg L-1; April), while
higher concentrations were for the lagoon (5.3-9.5 mg
L-1) in the wet and pre-dry seasons. According to an
adaptation of the Venice system used to describe
salinity zones in estuaries (Whitfield, 1998), the inlet
and channel areas are typically polyhaline, ranging
from 22.1 to 29.5, whereas the lagoon was significantly
different from mesohaline conditions (13). Seasonal
variations in salinity were recorded, ranging from
oligohaline (wet season; 3.3) to marine conditions (dry;
34.1). Water temperature and pH presented seasonal
variations, while the depth and water clarity only
showed changes between habitats. The habitat structure
score presented its highest mean value for the lagoon
(8.6), while the lowest value was obtained for the inlet
(3.3) (Table 1).
The PCA of the hydrological variables explained
63.6% of the variance for the first two axes (Fig. 2).
This model considered only four explanatory variables
after reducing multicollinearity. The PC1 contributed
with 36.8% of the explained variance and it was
strongly related (based on eigenvectors of correlation
matrix) with depth (-0.56) and salinity (-0.45); whereas,
the PC2 contributed with 26.8% of the explained
variance and better correlated with dissolved oxygen
(0.43) and pH (-0.41).
 Fish assemblages in a shallow lagoon-estuarine system 27

Table 1. Means (and standard deviation) of hydrological parameters in the La Joya-Buenavista lagoon-estuarine
system (Mexico), June 2013-April 2014, and results of the ANOVA (F) and Kruskal-Wallis test (H) analyses
for spatial and temporal comparisons for each parameter. Significant P-values (<0.05) are in bold. Seasons
having the same superscript letter were not significantly different within each temporality. Habitat structure
values also are presented. I: inlet; C: channel; L: lagoon.

Season Inlet Channel Lagoon Spatial Temporal

Water temperature (°C)
Pre-weta 31.4 (0.1) 32.0 (0.4) 33.1 (1.6) H = 2.99 F = 36.84
Weta 30.5 (0.1) 30.1 (1.3) 31.5 (2.5) P = 0.224 P = 0.000
Pre-dryb 28.6 (0.0) 27.5 (0.1) 25.8 (1.7)
Drya 30.7 (1.1) 32.6 (1.3) 32.3 (1.4)
Depth (cm)
Pre-wet 89.4 (0.4) 50.3 (4.2) 55.3 (16.1) H = 7.3 H = 3.21
Wet 66.3 (8.5) 82.7 (64.9) 80.5 (52.5) P = 0.026 P = 0.361
Pre-dry 147.5 (0.0) 181.4 (49.5) 73.2 (28.1) I, C > L
Dry 80.2 (77.5) 96.1 (35.7) 44.1(24.4)
Water clarity (cm)
Pre-wet 87.4 (0.2) 47.5 (4.2) 52.4 (16.1) H = 7.31 H = 3.21
Wet 66.3 (8.5) 40.0 (11.9) 55.4 (20.0) P = 0.026 P = 0.361
Hydrological parameters

Pre-dry 145.0 (1.8) 125.6 (49.5) 40.0 (18.1) I, C > L

Dry 69.5 (77.1) 86.3 (35.7) 44.5 (24.0)
Dissolved oxygen (mg L-1)
Pre-wetab 4.6 (0.1) 2.4 (1.0) 4.8 (1.2) F = 25.08 F = 4.45
Wetb 4.4 (0.0) 4.4 (0.5) 5.4 (1.4) P = 0.000 P = 0.006
Pre-dryab 3.4 (0.3) 2.5 (0.3) 6.5 (1.9) L > I, C
Dryac 1.9 (0.9) 2.4 (1.8) 4.6 (1.2)
Salinity
Pre-weta 31.9 (0.1) 20.3 (1.5) 14.1 (5.8) F = 8.37 F = 43.32
Wetb 23.6 (8.9) 16.7 (5.9) 3.3 (2.4) P = 0.006 P = 0.000
Pre-dryab 29.1 (0.6) 17.5 (2.1) 7.1 (2.3) I, C > L
Dryc 34.0 (0.5) 34.1 (0.4) 27.7 (5.6)
pH
Pre-weta 8.4 (0.1) 8.2 (1.0) 8.9 (1.0) F = 2.78 F = 10.37
Wetb 7.5 (0.5) 7.6 (0.3) 7.1 (0.7) P = 0.068 P = 0.000
Pre-drybc 7.4 (0.1) 7.6 (1.0) 7.7 (0.7)
Dryac 7.1 (1.2) 6.7 (0.3) 8.8 (0.8)
Inlet Channel Lagoon
Substrate 1.1 (0.1) 2.2 (0.2) 2.9 (0.2)
Vegetation 1.2 (0.3) 3.0 (0.0) 2.8 (0.5)
Shelter 1.1 (0.1) 2.1 (0.1) 2.9 (0.1)
Mean value 3.3 (0.4) 7.3 (0.4) 8.6 (0.5)

Fish assemblage structure According to the IV, 15 species together contribute

Two thousand sixty-four fish individuals were
collected by cast net (from 76 sampling events during
the study period) and were identified in 48 species and
21 families. The fish assemblage in the LJB was
dominated by Lile gracilis (13.91%), followed by
Astatheros macracanthus (10.08%) and Eucinostomus
currani (9.98%); only three species, Mugil curema,
Dormitator latifrons and Gerres simillimus contributed
with an amount as large as 36.78% of the total biomass.
75% of relative value (Table 2).
Although the LJB system showed a significant
environmental variation between seasons, the fish
fauna exhibited their main variations across habitat
types. The observed number of species per habitat was
35 in the lagoon, 20 in the inlet and 17 in the channel.
Significant differences were found between habitat
with the standardized richness [E (S1251)], ranging from
13 taxa (channel) to 26 taxa (lagoon) (H = 6.98, P <
28 Latin American Journal of Aquatic Research
Figure 2. Principal component analysis environmental
biplot, La Joya-Buenavista lagoon-estuarine system,
Mexico. The length and direction of the vectors represent
the strength of the relationship concerning a unit circle.
Symbols represent an individual sampling event coded by
season. Gray circles: pre-wet, gray inverted triangles: wet,
white circles: pre-dry, black triangles: dry.
0.05) (Fig. 3a). Differences were found between
seasons with the E (S710), ranging from 20 taxa (pre-
wet) to 33 taxa (pre-dry), although these were not
significant (F = 1.7, P > 0.05) (Fig. 3b).
Spatial and temporal variation of fish assemblages
The PERMANOVA results conducted showed that fish
assemblages differed significantly at the spatial level
(habitat, sampling site; P < 0.01). At the temporal level,
differences between seasons were also detected, but not
by month or their interactions (Table 3).
According to the SIMPER analysis, the average
dissimilarity among habitats ranged from 88.3 to
97.3%. Most of the dissimilarity between lagoon-inlet
and inlet-channel was due to the species E. currani
(14.7 and 16%, respectively), while Centropomus
robalito presented a high contribution (12.8%) in the
dissimilarity between the lagoon and channel (Table 4).
Regarding the functional guilds in the mouth and
lagoon, euryhaline species (X̄ = 61.8% ± 29.3) and
omnivores (X̄ = 58.8% ± 30.9) were dominant in
abundance, while estuarine residents (53.8%) and
zooplanktivores (44.1%) were more abundant in the
channel.
The mean fish size differed among the three habitats
(H = 62.26, P < 0.01). Standard length data showed that
some of the dominant taxa (A. macracanthus, M.
curema, E. currani, D. latifrons) were smaller in the
lagoon compared with other habitats according to the
Mann-Whitney test. In the case of Lutjanus
argentiventris, which was not captured in the lagoon,
the smaller specimens corresponded to the inlet. On the
Figure 3. Rarefaction curves of the expected number of
species as a function of sample size calculated by a) habitat
and b) season; La Joya-Buenavista lagoon-estuarine system,
Mexico. The bars indicate the subsample limits for the
number of species and specimens. For the standardized
richness values sharing the same letter were not
statistically different at P < 0.05 with the non-parametric
ANOVA and the Mann-Whitney post-hoc test.
other hand, L. gracilis and Atherinella guatemalensis
were species whose size does not differ between
habitats (Fig. 4).
Relationship between fish assemblages and
environmental parameters
The DistLM analysis identified four environmental
variables strongly correlated with the fish assemblages
when tested in isolation (marginal tests; Table 5).
However, in the best solution of the full model
(sequential tests, adjusted R2 = 0.48), only habitat
structure, salinity and depth together were enough to
explain significantly 43% of the total variance. Selected
variables by the step-wise procedure were displayed as
vectors in the dbRDA ordination plot (Fig. 5). Fish
assemblages modeled by four predictor variables
revealed two gradients. The first gradient was related to
habitat structure and salinity, which kept inlet sites
separated from lagoon and channel sites. The second
gradient was mainly driven by dissolved oxygen and
 Fish assemblages in a shallow lagoon-estuarine system 29

Table 2. Relative importance value of the fish species for the La Joya-Buenavista lagoon-estuarine system (Mexico).
Relative values based on the total number of specimens (2,064), total biomass (17,027.83 g) and the number of sampled
sites (13). n: numerical abundance; SL: size ranges in standard length; %n: relative abundance; %B: relative biomass; %F:
relative frequency; %IV: relative importance value.

Family Specie n SL (cm) %n %B %F %IV

Clupeidae Lile gracilis Castro-Aguirre & Vivero, 1990 287 3.3-8.2 13.91 5.52 6.42 8.61
Cichlidae Astatheros macracanthus (Günther, 1864) 208 2.1-13.4 10.08 9.44 5.88 8.47
Mugilidae Mugil curema Valenciennes, 1863 129 4.3-21.7 6.25 12.41 4.28 7.65
Gerreidae Eucinostomus currani Zahuranec, 1980 206 1.5-9.5 9.98 8.13 4.81 7.64
Eleotridae Dormitator latifrons (Richardson, 1844) 115 1.7-15.7 5.57 14.34 2.67 7.53
Gerreidae Gerres simillimus Regan, 1907 82 1.9-18.3 3.97 10.03 5.35 6.45
Gerreidae Diapterus brevirostris (Sauvage, 1879) 113 2.3-8.8 5.47 5.90 6.42 5.93
Poeciliidae Poecilia nelsoni (Meek, 1904) 200 1.7-5.1 9.69 2.30 3.21 5.07
Centropomidae Centropomus robalito Jordan & Gilbert, 1882 121 3.1-16.7 5.86 3.48 4.28 4.54
Cichlidae Amphilophus trimaculatus (Günther, 1867) 81 2.3-12.7 3.92 1.54 3.21 2.89
Atherinopsidae Atherinella guatemalensis (Günther, 1864) 63 1.6-6.5 3.05 0.15 4.28 2.49
Carangidae Oligoplites altus (Günther, 1868) 16 6.5-18.7 0.78 2.95 2.67 2.13
Poeciliidae Poecilia sphenops Valenciennes, 1846 75 2.0-5.1 3.63 1.14 1.07 1.95
Engraulidae Anchoa mundeola (Gilbert & Pierson, 1898) 26 4.0-8.4 1.26 0.60 3.74 1.87
Gobiidae Gobionellus microdon (Gilbert, 1892) 23 5.3-15.0 1.11 1.19 3.21 1.84
Eleotridae Gobiomorus maculatus (Günther, 1859) 29 7.5-14.1 1.41 2.58 1.07 1.68
Clupeidae Opisthonema libertate (Günther, 1867) 47 5.2-7.9 2.28 1.18 1.07 1.51
Gerreidae Eugerres axillaris (Günther,1864) 9 7.3-14.1 0.44 1.53 2.14 1.37
Centropomidae Centropomus armatus Gill, 1863 20 6.3-14.4 0.97 1.49 1.60 1.36
Atherinopsidae Membras gilberti (Jordan & Bollman, 1890) 27 8.3-11.1 1.31 1.49 1.07 1.29
Gerreidae Eugerres lineatus (Humboldt, 1821) 9 6.3-7.5 0.44 0.64 2.67 1.25
Carangidae Caranx caninus Günther, 1867 10 4.0-13.4 0.48 1.01 2.14 1.21
Centropomidae Centropomus nigrescens Günther, 1864 15 4.7-9.6 0.73 0.64 2.14 1.17
Lutjanidae Lutjanus argentiventris (Peters, 1869) 14 5.1-10.3 0.68 1.09 1.60 1.12
Engraulidae Anchoa lucida (Jordan & Gilbert, 1882) 15 5.3-8.7 0.73 0.39 2.14 1.08
Lutjanidae Lutjanus novemfasciatus Gill, 1862 10 4.2-9.4 0.48 0.51 2.14 1.04
Mugilidae Mugil cephalus Linnaeus, 1758 2 13.0-23.4 0.10 1.45 1.07 0.87
Ariidae Ariopsis guatemalensis (Günther, 1864) 15 3.4-8.1 0.73 0.21 1.60 0.85
Hemiramphidae Hyporhamphus naos Banford & Collette, 2001 5 17.4-22.5 0.24 1.19 1.07 0.83
Poeciliidae Poeciliopsis fasciata (Meek, 1904) 14 1.6-2.2 0.68 0.02 1.60 0.77
Engraulidae Anchovia macrolepidota (Kner, 1863) 15 6.5-14.3 0.73 1.01 0.53 0.76
Paralichthyidae Citharichthys gilberti Jenkins & Evermann, 1889 7 5.8-14.1 0.34 0.72 1.07 0.71
Clupleidae Lile nigrofasciata Castro-Aguirre, Ruiz-Campos & Balart, 2002 12 6.2-7.4 0.58 0.32 1.07 0.66
Carangidae Oligoplites saurus (Bloch & Schneider, 1801) 4 10.3-14.5 0.19 0.62 1.07 0.63
Ariidae Cathorops liropus (Bristol, 1897) 3 12.2-13.7 0.15 0.63 1.07 0.61
Lutjanidae Lutjanus colorado Jordan & Gilbert, 1882 2 8.9-15.8 0.10 0.60 1.07 0.59
Centropomidae Centropomus viridis Lockington, 1877 5 5.6-11.0 0.24 0.31 1.07 0.54
Tetraodontidae Sphoeroides annulatus (Jenyns, 1842) 3 4.5-5.2 0.15 0.14 1.07 0.45
Ariidae Cathorops steindachneri (Gilbert & Starks, 1904) 4 4.7-5.5 0.19 0.06 1.07 0.44
Achiridae Achirus mazatlanus (Steindachner, 1869) 3 3.1-3.8 0.15 0.02 1.07 0.41
Poeciliidae Poeciliopsis pleurospilus (Günther, 1866) 9 1.8-3.2 0.44 0.05 0.53 0.34
Anablepidae Anableps dowei Gill, 1861 3 6.6-11.5 0.15 0.26 0.53 0.31
Mugilidae Mugil hospes Jordan & Culver, 1865 2 8.3-10.2 0.10 0.23 0.53 0.29
Haemulidae Haemulopsis axillaris (Steindachner, 1869) 1 10.8 0.05 0.21 0.53 0.26
Haemulidae Orthopristis chalceus (Günther, 1864) 1 10.1 0.05 0.19 0.53 0.26
Labridae Halichoeres dispilus (Günther, 1864) 1 8.4 0.05 0.07 0.53 0.22
Gobiidae Aboma etheostoma Jordan & Starks, 1895 2 1.7-1.8 0.10 0.00 0.53 0.21
Characidae Astyanax aeneus (Günther, 1860) 1 4.6 0.05 0.02 0.53 0.20
30 Latin American Journal of Aquatic Research

Table 3. Results of PERMANOVA based on Bray-Curtis dissimilarities on fish abundance data in response to season,
habitat, months, sampling sites, and their interactions in the La Joya-Buenavista lagoon-estuarine (LJB) system (Mexico).
d.f.: degrees of freedom, MS: mean square; F: pseudo-F statistic value, P: P-values by permutation. Permutated residuals
under a reduced model (Type III). The maximum number of permutations = 9,999. Significant P-values (<0.05) are in bold.

Source of variation d.f. MS F P

Habitat (Ha) 2 25960 11.24 0.0001
Season (Se) 3 5438.5 2.35 0.002
Sampling site (Si, nested in Ha) 10 3748.1 1.62 0.008
Month (Mo, nested in Se) 2 2397 1.04 0.426
Ha × Se 6 5098.3 2.21 0.0004
Ha × Mo 4 2314.3 1.00 0.474
Se × Si 30 2459.6 1.06 0.348
Residuals 20 2310

Table 4. Discrimination of 10 fish species based on its relative contribution among habitats by SIMPER analysis; La Joya-
Buenavista lagoon-estuarine (LJB) system (Mexico). Ecological category: E: estuarine resident, EU: marine euryhaline,
ST: marine stenohaline, SF: secondary freshwater. Functional group: DV: detritivore, OV: omnivore, PV: piscivore, ZB:
zoobenthivore, ZP: zooplanktivore, I: inlet, C: channel, L: lagoon.

Ecological Functional Spatial distribution Contribution (%)

Species
category group I C L L vs I L vs C I vs C
Eucinostomus currani EU OV 14.66 3.52 16.01
Centropomus robalito EU PV 2.35 12.79 10.02
Diapterus brevirostris EU OV 7.09 6.72 5.68
Lile gracilis E ZP 5.72 8.62 2.49
Astatheros macracanthus SF OV 4.88 7.62 4.43
Dormitator latifrons E DV - 8.86 6.47
Atherinella guatemalensis E ZB 7.55 - 6.90
Lutjanus argentiventris ST PV 5.17 - 4.78
Gerres simillimus EU OV 4.65 5.86 -
Mugil curema EU DV 4.58 2.93 2.99

depth, discriminating against the lagoon sites from the
channel sites.
DISCUSSION
The specific richness in the LJB system (48 species)
was higher than that described in other ecological
studies carried out in the Gulf of Tehuantepec. In the
southern Gulf, richness varied between 31 species in
the Chantuto-Panzacola system (Díaz-Ruiz et al., 2004)
and 40 in Carretas-Pereyra (Velázquez-Velázquez et
al., 2008). However, in the first case, comparisons
between the fish assemblages should be taken with
caution, due to the difference in the sampling effort and
method. In the second case, the sampling was more
comparable with this study, and differences in richness
and composition may be due to less marine influence
due to mouth dynamics (Gómez-González et al., 2012).
Although it has been pointed out that the use of a single
fishing gear results in a biased sample of the
assemblage (Clement et al., 2014), in estuarine
wetlands the use of cast nets is highly effective for
achieving a broad taxonomic representation in several
shallow habitats, and with accurate estimate of
abundances (Sheaves et al., 2007; Sheaves & Johnston,
2009). However, highly complex habitats should be
explored to avoid underrepresenting the cryptic fish
fauna.
According to our hypothesis, we found that the fish
fauna varied significantly within each geomorphic
habitat. When abundances of 48 species at 72 sampling
events are ordered on the two primary axes of dbRDA
(Fig. 5), a spatial pattern response in fish assemblages
on the lagoon, inlet and the channel is identified (Table
4; Fig. 3, 5). The lagoon exhibits a greater richness (35
spp.) with smaller sizes, compared to the inlet (20 spp.)
and the channel (17 spp.), suggesting differentiated use
of the habitat or the existence of assemblages with their
ecological attributes. The above could also be reflected
in the percentages of the functional guilds in each
habitat (e.g., a greater number of omnivores in the
lagoon; Table 4).
 Fish assemblages in a shallow lagoon-estuarine system 31

Figure 4. Standard length distribution of 10 species identified by SIMPER. Within species, the distributions sharing the
same letter were not significantly different on P < 0.05 with the non-parametric ANOVA and the Mann-Whitney pairwise
test.

Table 5. Marginal and sequential tests result for the

distance-based linear models based on fish abundance data
in the La Joya-Buenavista lagoon-estuarine (LJB) system
(Mexico). SS: sum of squares; F: pseudo-F statistic value;
P: P-value of permutation test for the relationship between
the fish assemblages and environmental parameters.
Significant P-values (<0.05) are in bold.

Variable SS trace F P
Marginal test
Habitat structure 11536 4.25 0.001
Depth 6417 2.17 0.036
Dissolved oxygen 6163 2.02 0.042
Salinity 6088 1.99 0.046
Water clarity 4375 1.38 0.209
pH 3694 1.15 0.300
Water temperature 1799 0.54 0.847
Figure 5. Distance-based redundancy analysis biplot
Sequential test
based on linear modelling for fish abundance data, La
Joya-Buenavista lagoon-estuarine system, Mexico. Vectors Habitat structure 11536 4.25 0.001
indicate correlations between the four environmental Depth 6713 2.74 0.009
parameters of most significance in the model and the axes. Salinity 4091 1.76 0.050
The length and direction of the vectors represent the
strength of the relationship concerning a unit circle. spatial patterns were described by França et al. (2009)
Symbols represent an individual sampling event coded by and Neves et al. (2013) in temperate and tropical
habitat. Black triangles: inlet, gray squares: channel, white coastal lagoons. If the habitats offer differentiated
circles: lagoon. resources in food and shelter, the sequential use of these
In the LJB system, the connectivity among the three will favor an efficient use of the lagoon-estuarine
geomorphic habitats may be a key attribute that defines system as a whole (Abrantes et al., 2015; Loureiro et
the small-scale variation of fish assemblages. Similar al., 2016). Also, the results obtained here are consistent
32 Latin American Journal of Aquatic Research
with the theory that the seascape/landscape structure
plays a determinant role in the structure of fish
assemblages (Kimirei et al., 2013).
Although differences were found at the temporal
level, the spatial variations among geomorphic habitats
were more significant (Table 3), probably due to a
higher number of dominant species residing into the
system during the entire annual cycle, and whose
movements depend on the availability of resources
(Lukey et al., 2006; Herzka et al., 2009). Another
explanatory factor could be the relative environmental
stability of the system. The significant spatio-temporal
interactions detected, habitat  season and between
sampling sites, can be indicative of seasonal pulses that
define variations in physical and chemical properties
within the same ecological or spatial unit (Yáñez-
Arancibia et al., 1983; Roselli et al., 2013). However,
the lowest relationship found at a temporal scale could
be because only one annual cycle was evaluated.
Therefore, a study in time series would be required to
corroborate these results.
The presence of large areas of complex habitats, like
mangroves, is a key factor why fish use lagoon
estuarine systems as nurseries. Mangroves support
more diverse and abundant small-sized fish
assemblages, as they favor greater protection from
predators and increase food availability (Nagelkerken
et al., 2002; Hindell & Jenkins, 2004; Piko &
Szedlmayer, 2007; Green et al., 2012; Neves et al.,
2013). The sheltered lagoon and the riverine mangroves
that border the channel are suitable habitats for the fish
fauna in the LJB system. However, during the dry
season, the mangrove root system is not available for
fishes; thus, the lack of physical structure may result in
a reduction of shelter. Therefore, the highest abundance
and richness of species in the lagoon, compared with
the other habitats, suggests that this area has a
significant ecological value. In this order, Franco et al.
(2006) and Verdiell-Cubedo et al. (2013) have reported
high abundance values in shallow habitats with small
patches of macrophytes or perimetral lagoon
marshlands, suggesting that juvenile fish use open-
lagoon areas for feeding (Arceo-Carranza & Chiappa-
Carrara, 2013; Kathoon et al., 2014). The high
abundance of species with detritivore, zoobenthivore
and zooplanktivore feeding habits (e.g., Mugil curema,
Lile gracilis, Atherinella guatemalensis) were recorded
in the lagoon area (Table 4), suggesting that both the
physical and biotic attributes of this habitat influenced
the population traits of these species.
The proximity of mangroves and mixed substrates
also contributes to increasing the complexity of the
channel; however, this habitat presented less abundance
and richness concerning the inlet, considered of low
complexity (Lacerda et al., 2014). However, it has been
reported that in tropical estuaries, there are lower values
of abundance and richness associated with the mouth
area (Neves et al., 2013). Even though, in our study, the
inlet is the richest species area of all estuarine channel,
which may be due to the occurrence of rare species,
mainly of stenohaline affinity (Peralta-Meixueiro &
Vega-Cendejas, 2011), during the pre-dry and dry
seasons. During the rainy season, freshwater inputs
modify the hydrology (salinity, dissolved oxygen,
temperature), with a higher number of estuarine species
attracted to the beach by a high density of such prey
(e.g., Litopenaeus spp.). On the other hand, during the
dry season, the beach environment becomes similar to
the marine zone, with a lower abundance of fish but a
higher richness and dominance of some families (e.g.,
Carangidae and Sciaenidae).
A meaningful relationship has been founded for
several environments between the habitat complexity
and the structure of animal assemblages. The ecological
paradigm holds that the most complex and physically
heterogeneous habitats will support more diverse
communities (Stewart et al., 2000). An increase in
available refuges due to microtopographic variations of
the substrate or physical structures also has been shown
to reduce inter and intra-specific competition for space,
which potentially increases the richness and abundance
of fish (Almany, 2004; Consoli et al., 2018).
Some of the dominant species found in the lagoon
and the channel are secondary freshwater and estuarine
residents (e.g., Dormitator latifrons and Astatheros
macracanthus). The distribution and population
structure of this group are determined by a temporal
pattern affecting hydrological conditions (Díaz-Ruiz et
al., 2004; Velázquez-Velázquez et al., 2008). During
the rains, larger organisms were found in the channel,
while juveniles of these species occurred in the lagoon
during the pre-dry and dry seasons, suggesting a local
migration from the streams to mesohaline environ-
ments.
In the LJB system, families such as Gerreidae and
Mugilidae present greater abundances of larger
organisms in the inlet than in the lagoon, suggesting
that the sandy bars play an important and specific role
for providing habitat. For example, in northern
Australia, Blaber et al. (1995) found that the tidal
environment, located between the mouth of an open
estuary and the adjacent lower marine zone, sustains a
relatively complex fish assemblage, composed by
dependent juveniles as well as groups of opportunistic
species that are move through three habitats (estuary,
inshore and offshore waters). The structure of a similar
assemblage occurs in the inlet of the LJB system, where
juveniles of some species (e.g., Lutjanus argentiventris)
 Fish assemblages in a shallow lagoon-estuarine system
were found exclusively in this area, and others of
distribution extended by all habitats without variations
in their size (e.g., L. gracilis).
Water depth could be a parameter strongly
correlated to abundance and size structure in the biotic
assemblages of an estuarine system. A general pattern
observed shows that larger fishes will be more
abundant in deeper habitats, whereas smaller ones will
be more abundant in shallow environments
(Hutchinson et al., 2014; Mustamäki et al., 2015;
Becker et al., 2017). In the LJB system, the greatest
depths were recorded in the channel, which may
explain the occurrence of larger specimens from
families as Lutjanidae, Centropomidae and Cichlidae
(Fig. 4); this habitat could be used as a transit or feeding
zone in mangroves and marginal lowlands. Hypoxia
and low-depth are significant barriers to the presence of
larger predatory fish in the lagoon. They affect their
ability to move and evade predation, due to
physiological stress (Patterson & Whitfield, 2000;
Shoji et al., 2005), so greater impact towards recruits
will be inflicted by small and juvenile piscivores (Baker
& Sheaves, 2009); further evidence for a specific
trophic structure for each habitat in the environment
(Tecchio et al., 2015).
Although there were seasonal differences, the
evidence of fish-habitat associations for many species
was broad regardless of seasonality, probably because
a high percentage of resident species in the system was
found during the annual cycle. However, sampling
needs to be expanded to compare contiguous systems
and between-year variations in order to corroborate
these conclusions. Several anthropogenic pressures are
affecting the lagoon estuaries of the Gulf of
Tehuantepec, whose vulnerability has increased in
recent years as a result of the lack of planning in the
coastal basin. Due to their ability to respond to
environmental changes, fish assemblages are a
potential tool for monitoring the ecological integrity of
coastal systems, so their study should be continued.
Likewise, coastal management should be developed to
conserve the mosaic of habitats that integrate all the
system, rather than distinct habitats.
ACKNOWLEDGMENTS
We thank the Cooperative Society of Fish Production
“Miguel Hidalgo y Costilla” for their participation in
the collection data. The authors would also like to thank
Manuel Anzueto and Eduardo Urbina for their field and
lab technical assistance. Comments on a manuscript
from Wilfredo Matamoros helped to improve the final
version substantially. This paper is part of the first
author’s Doctor of Science dissertation at the Univer-
33
sidad Nacional Autónoma de México (UNAM). The
Mexican Consejo Nacional de Ciencia y Tecnología
(CONACYT) granted a scholarship to the first author.
REFERENCES
Abrantes, K.G., Barnett, A., Baker, R. & Sheaves, M.
2015. Habitat-specific food webs and trophic
interactions supporting coastal-dependent fishery
species: an Australian case study. Reviews in Fish
Biology and Fisheries, 25(2): 337-363. doi: 10.1007/
s11160-015-9385-y
Almany, G.R. 2004. Does increased habitat complexity
reduce predation and competition in coral reef fish
assemblages? Oikos, 106: 275-284.
Anderson, M.J. 2001. A new method for non-parametric
multivariate analysis of variance. Australian Journal of
Ecology, 26: 32-46. doi: 10.1111/j.1442-9993.2001.
01070.pp.x
Anderson, M.J. 2006. Distance-based tests for homo-
geneity of multivariate dispersions. Biometrics, 62:
245-253.
Anderson, M.J., Gorley, R.N. & Clarke, K.R. 2008.
PERMANOVA+ for PRIMER: guide to software and
statistical methods. PRIMER-E, Plymouth.
Arceo-Carranza, D. & Chiappa-Carrara, X. 2013. Feeding
ecology of juvenile marine fish in a shallow coastal
lagoon of south-eastern Mexico. Latin American
Journal of Aquatic Research, 43(4): 621-631. doi:
10.3856/vol43-issue4-fulltext-1
Ayala-Pérez, L.A., Vasco-Villa, O. & Sosa-López, A.
2014. Evaluación de las asociaciones de peces
dominantes influenciadas por el ciclo nictemeral y la
variación temporal en la Reserva de la Biósfera Los
Petenes, Campeche, México. Ciencia UAT, 9(1): 33-
43.
Baker, R. & Sheaves, M. 2009. Overlooked small and
juvenile piscivores dominate shallow-water estuarine
“refuges” in tropical Australia. Estuarine, Coastal and
Shelf Science, 85(4): 618-626. doi: 10.1016/j.ecss.
2009.10.006
Bakun, A., Csirke, J., Lluch-Belda, S. & Steer-Ruiz, R.
1999. The Pacific Central American Coastal LME. In:
Sherman, K. & Tang, Q. (Eds.). Large marine
ecosystems of the Pacific Rim. Blackwell Science,
Cambridge, pp. 268-280.
Bartholomew, A., Diaz, R.J. & Cicchetti, G. 2000. New
dimensionless indices of structural habitat complexity:
predicted and real effects on a predator´s foraging
success. Marine Ecology Progress Series, 206: 45-58.
doi: 10.3354/meps206045
Becker, A., Whitfield, A.K., Cowley, P.D. & Cole, V.J.
2017. Does water depth influence the size composition
of estuary-associated fish? Distributions revealed
34 Latin American Journal of Aquatic Research
using mobile acoustic-camera transect along the
channel of a small shallow estuary. Marine and
Freshwater Research, 68: 2163-2169. doi: 10.1071/
MF16230
Blaber, S.J.M., Brewer, D.T. & Salini, J.P. 1995. Fish
communities and the nursery role of the shallow
inshore waters of a tropical bay in the Gulf of
Carpenteria, Australia. Estuarine, Coastal and Shelf
Science, 40: 177-193. doi: 10.1016/S0272-7714(05)
80004-6
Castillo-Rivera, M., Zárate-Hernández, R., Ortiz-Burgos,
S. & Zavala-Hurtado, J. 2010. Diel and seasonal
variability in the fish community structure of a mud-
bottom estuarine habitat in the Gulf of Mexico. Marine
Ecology, 31: 633-642. doi: 10.1111/j.1439-0485.2010.
00394.x
Castro-Aguirre, J.L., Espinosa-Pérez, H.S. & Schmitter-
Soto, J.J. 1999. Ictiofauna estuarino-lagunar y vicaria
de México. Limusa-Noriega, Ciudad de México.
Clarke, K.R. 1993. Non-parametric multivariate analyses
of changes in community structure. Australian Journal
of Ecology, 18: 117-143. doi: 10.1111/j.1442-9993.
1993.tb00438.x
Clarke, K.R. & Gorley, R.N. 2006. PRIMER 6: user
manual-tutorial. PRIMER-E, Plymouth.
Clement, T.A., Pangle, K., Uzarski, D.G. & Murray, D.A.
2014. Effectiveness of fishing gears to assess fish
assemblage size structure in small lake ecosystems.
Fisheries Management and Ecology, 21: 211-219. doi:
10.1111/fme.12069
Colwell, R.K., Chao, A., Gotelli, N.J., Lin, S., Mao, C.X.,
Chazdon, R.L. & Longino, J.T. 2012. Models and
estimators linking individual-based and sample-based
rarefaction, extrapolation, and comparison of assem-
blages. Journal of Plant Ecology, 5(1): 3-21. doi:
10.1093/jpe/rtr044
Consoli, P., Mangano, M.C., Sarà, G., Romeo, T. &
Andaloro, F. 2018. The influence of habitat complexity
on fish assemblages associated with extractive
platforms in the central Mediterranean Sea. Advances
in Oceanography and Limnology, 9(2): 59-67. doi:
10.4081/aiol.2018.7918
Contreras, E.F. 2010. Ecosistemas costeros mexicanos: una
actualización. Universidad Autónoma Metropolitana,
Unidad Iztapalapa, Ciudad de México.
Contreras, E.F. & Zabalegui, M.LM. 1991. Hidrología,
nutrientes y productividad primaria en la laguna La
Joya-Buenavista, Chiapas, México. Anales del
Instituto de Ciencias del Mar y Limnología, 18(2):
207-215.
Day Jr., J.W., Hall, C.A.S., Kemp, W.M., Yáñez-
Arancibia, A. & Crump, B.C. (Eds.). 2012. Estuarine
ecology. Wiley-Blackwell, New York.
Díaz-Ruiz, S., Cano-Quiroga, E., Aguirre-León, A. &
Ortega-Bernal, R. 2004. Diversidad, abundancia y
conjuntos ictiofaunisticos del sistema lagunar-
estuarino Chantuto-Panzacola, Chiapas, México.
Revista de Biología Tropical, 52(1): 187-199. doi:
10.15517/ RBT.V52I1.14879
Elliott, M., Whitfield, A.K., Potter, I.C., Blaber, S.J.M.,
Cyrus, D.P., Nordlie, F.G. & Harrison, T.D. 2007. The
guild approach to categorizing estuarine fish
assemblages: a global review. Fish and Fisheries, 8:
241-268. doi: 10.1111/j.1467-2679.2007.00253.x
França, S., Costa, M.J. & Cabral, H.N. 2009. Assessing
habitat-specific fish assemblages in estuaries along the
Portuguese coast. Estuarine, Coastal and Shelf
Science, 83: 1-12. doi: 10.1016/j.ecss.2009.03.013
França, S., Vasconcelos, R.P., Fonseca, V.F., Tanner,
S.E., Reis-Santos, P., Costa, M.J. & Cabral, H.N.
2012. Predicting fish community properties within
estuaries: influence of habitat type and other
environmental features. Estuarine, Coastal and Shelf
Science, 107: 22-31. doi: 10.1016/j.ecss.2012.04.013
Franco, A., Torricelli, P. & Franzoi, P. 2009. A habitat-
specific fish-based approach to assess the ecological
status of Mediterranean coastal lagoons. Marine
Pollution Bulletin, 58: 1704-1717. doi: 10.1016/
j.marpolbul.2009.06.016
Franco, A., Franzoi, P., Malavasi, S., Riccato, F.,
Torricelli, P. & Mainardi, D. 2006. Use of shallow
water habitats by fish assemblages in a Mediterranean
coastal lagoon. Estuarine, Coastal and Shelf Science,
66: 67-83. doi: 10.1016/j.ecss.2005.07.020
Fricke, R., Eschmeyer, W.N. & Van der Laan, R. (Eds.).
2019. Eschmeyer´s catalog of fishes: genera, species,
references. California Academy of Sciences,
California. [http://researcharchive.calacademy.org/
research/ichthyology/catalog/fishcatmain.asp]. Revie-
wed: Jun 28, 2019.
Froese, R. & Pauly, D. 2016. FishBase. [www.
fishbase.org]. Reviewed: October 16, 2016.
Gómez-González, A.E., Velázquez-Velázquez, E., Rodiles-
Hernández, R., González-Díaz, A.A., González-Acosta,
A.F. & Castro-Aguirre, J.L. 2012. Lista sistemática de
la ictiofauna en la Reserva de la Biosfera La
Encrucijada, Chiapas, México. Revista Mexicana de
Biodiversidad, 83: 674-686. doi: 10.7550/rmb.24468
González-Acosta, A.F., Rodiles-Hernández, R. &
González-Díaz, A.A. 2017. Checklist of the marine
and estuarine fishes of Chiapas, Mexico. Marine
Biodiversity, 48: 1439-1454. doi: 10.1007/s12526-
016-0630-y
 Fish assemblages in a shallow lagoon-estuarine system
Green, B.C., Smith, D.J. & Underwood, G.J.C. 2012. Habitat
connectivity and spatial complexity differentially
affected mangrove and salt marsh fish assemblages.
Marine Ecology Progress. Series, 466: 177-192. doi:
10.3354/meps09791
Griffiths, S.P. 2001. Factors influencing fish composition
in an Australian intermittently open estuary. Is
stability salinity-dependent? Estuarine, Coastal and
Shelf Science, 52: 739-751. doi: 10.1006/ecss.2000.
0756
Herzka, S.Z., Griffiths, R., Fodrie, F.J. & McCarthy, I.D.
2009. Short-term size-specific distribution and
movement patterns of juvenile flatfish in a Pacific
estuary derived through length-frequency and mark-
recapture data. Ciencias Marinas, 35: 41-57.
Hicks, A., Barbee, N.C., Swearer, S.E. & Downes, B.J.
2010. Estuarine geomorphology and low salinity
requirement for fertilization influence spawning site
location in the diadromous fish, Galaxias maculatus.
Marine and Freshwater Research, 61(11): 1252-1258.
doi: 10.1071/MF10011
Hindell, J.S. & Jenkins, G.P. 2004. Spatial and temporal
variability in the assemblage structure of fishes
associated with mangroves (Avicennia marina) and
intertidal mudflats in temperate Australian
embayments. Marine Biology, 144: 385-395. doi:
10.1007/s00227-003-1201-x
Hutchinson, N., Jenkins, G.P., Smith, T.M. & Brown, A.
2014. Variation with depth in temperate seagrass-
associated fish assemblages in southern Victoria,
Australia. Estuaries and Coasts, 37: 801-814. doi:
10.1007/s12237-013-9742-9
Kathoon, Z., Paperno, R. & Makhdoom-Hussain, S. 2014.
Spatial and temporal changes in the fish communities
from a mangrove-dominated creek system near
Karachi, Pakistan. Journal of Applied Ichthyology, 30:
350-358. doi: 10.1111/jai.12377
Kimirei, I.A., Nagelkerken, I., Mgaya, Y.D. & Huijbers,
C.M. 2013. The mangrove nursery paradigm revisited:
otolith stable isotopes support nursery-to-reef
movements to Indo-Pacific fishes. Plos One, 8(6):
e66320. doi: 10.1371/journal.pone.0066320
Krebs, C.J. 1999. Ecological methodology. Addison-
Wesley, California.
Lacerda, C.H.F., Barletta, M. & Dantas, D.V. 2014.
Temporal patterns in the intertidal faunal community
at the mouth of a tropical estuary. Journal of Fish
Biology, 85: 1571-1602. doi: 10.1111/jfb.12518
Lankford, R.R. 1977. Coastal lagoons of Mexico. Their
origin and classification. In: Wiley, M. (Ed.).
Estuarine processes. Circulation, sediments, and
35
transfer of material in the estuary. Academic Press,
New York, pp. 182-215.
Legendre, P. & Anderson, M.J. 1999. Distance-based
redundancy analysis: testing multispecies responses to
multifactorial ecological experiments. Ecological
Monographs, 69: 1-24. doi: 10.2307/2657192
Loureiro, S.N., Reis-Filho, J.A. & Giarrizzo, T. 2016.
Evidence for habitat-driven segregation of an estuarine
fish assemblage. Journal of Fish Biology, 89: 804-820.
doi: 10.1111 /jfb.13017
Lukey, J.R., Booth, A.J. & Froneman, P.W. 2006. Fish
population size and movement patterns in a small
intermittently open South African estuary. Estuarine,
Coastal and Shelf Science, 67: 10-20. doi:
10.1016/j.ecss.2005.10.021
McArdle, B.H. & Anderson, M.J. 2001. Fitting
multivariate models to community data: a comment on
distance-based redundancy analysis. Ecology, 82: 290-
297. doi: 10.2307/2680104
McLusky, D.S. & Elliott, M. 2004. The estuarine
ecosystem: ecology, threats and management.
University Press, Oxford.
Mendoza, E., Castillo-Rivera, M., Zárate-Hernández, R.
& Ortiz-Burgos, S. 2009. Seasonal variations in the
diversity, abundance, and composition of species in an
estuarine fish community in the Tropical Eastern
Pacific, Mexico. Ichthyological Research, 56: 330-
339. doi: 10.1007/s10228-009-0102-5
Mustamäki, N., Jokinen, H., Scheinin, M., Bonsdorff, E.
& Mattila, J. 2015. Seasonal small-scale variation in
distribution among depth zones in a coastal Baltic Sea
fish assemblage. ICES Journal of Marine Science,
72(8): 2374-2384. doi: 10.1093/icesjms/fsv068
Myers, G.S. 1966. Derivation of the freshwater fish fauna
of Central America. Copeia, 1966(4): 733-766.
Nagelkerken, I. & Van der Velde, G. 2002. Do non-
estuarine mangroves harbor higher densities of
juvenile fish than adjacent shallow-water and coral
reef habitats in Curaçao (Netherlands Antilles)?
Marine Ecology Progress Series, 245: 191-204. doi:
10.3354/meps 245191
Neves, L.M., Teixeira, T.P. & Araújo, F.G. 2011.
Structure and dynamics of distinct fish assemblages in
three reaches (upper, middle and lower) of an open
tropical estuary in Brazil. Marine Ecology, 32: 115-
131. doi: 10.1111/j.1439-0485.2010.00407.x
Neves, L.M., Teixeira, T.P., Franco, T.P., Pereira, H. &
Araújo, F.G. 2013. Fish composition and assemblage
structure in the estuarine mixing zone of a tropical
estuary: comparisons between the main channel and an
36 Latin American Journal of Aquatic Research
adjacent lagoon. Marine Biology Research, 9(7): 661-
675. doi: 10.1080/17451000.2013.765575
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P.,
Minchin, P.R., O´Hara, R.B., Simpson, G.L., Solymos,
P., Stevens, M.H.M. & Wagner, H. 2014. Vegan:
community ecology package, version 2.2. [http://
vegan.r-force.r-project.org]. Reviewed: June 12, 2016.
Ortega-García, S., Trigueros-Salmerón, J.A., Rodríguez-
Sánchez, R., Lluch-Cota, S. & Villalobos, H. 2000. El
Golfo de Tehuantepec como un centro de actividad
biológica y su importancia en las pesquerías. In:
Lluch-Belda, D., Elorduy-Garay, J., Lluch-Cota, S. &
Ponce-Díaz, G. (Eds.). BAC: centros de actividad
biológica en el Pacífico Mexicano. Centro de
Investigaciones Biológicas del Noroeste S.C., La Paz,
pp. 335-356.
Patterson, A.W. & Whitfield, A.K. 2000. Do shallow-
water habitats function as refugia for juvenile fishes?
Estuarine, Coastal and Shelf Science, 51: 359-364.
doi: 10.1006/ ecss.2000.0640
Peralta-Meixueiro, M.A. & Vega-Cendejas, M.E. 2011.
Spatial and temporal structure of fish assemblages in a
hyperhaline coastal system: Ría Lagartos, Mexico.
Neotropical Ichthyology, 9(3): 673-682. doi: 10.1590/
S1679-62252011005000033
Pérez-Ruzafa, A., Monpéan, C. & Marcos, C. 2007.
Hydrographic, geomorphologic and fish assemblage
relationship in coastal lagoons. Hydrobiologia, 577(1):
107-125. doi: 10.1007/978-1-4020-6008-3_10
Piko, A.A. & Szedlmayer, S.T. 2007. Effects of habitat
complexity and predator exclusion on the abundance
of juvenile red snapper. Journal of Fish Biology, 70:
758-769. doi: 10.1111/j.1095-8649.2007.01336.x
R Development Core Team. 2014. R: a language and
environment for statistical computing version 3.1.2. R
Foundation for Statistical Computing. [http://r-
project.org]. Reviewed: June 12, 2016.
Rodríguez-Romero, J., López-González, L.C., Galván-
Magaña, F., Sánchez-Gutiérrez, F.J., Inohuye-Rivera,
R.B. & Pérez-Urbiola, J.C. 2011. Seasonal changes in
a fish assemblage associated with mangroves in a
coastal lagoon of Baja California Sur, Mexico. Latin
American Journal of Aquatic Research, 39(2): 250-
260. doi: 10.3856/vol39-issue2-fulltext-6
Roselli, L., Cañedo-Argüelles, M., Goela, P.C., Cristina,
S., Rieradevall, M., DʼAdamo, R. & Newton, A. 2013.
Do physiography and hydrology determine the
physicochemical properties and trophic status of
coastal lagoons? A comparative approach. Estuarine,
Coastal and Shelf Science, 117: 29-36. doi: 10.1016/
j.ecss.2012.09.014
Saintilan, N. 2004. Relationships between estuarine
geomorphology, wetland extent and fish landings in
New South Wales estuaries. Estuarine, Coastal and
Shelf Science, 61: 591-601. doi: 10.1016/j.ecss.2004.
07.002
Sheaves, M. & Johnston, R. 2009. Ecological drivers of
spatial variability among fish fauna of 21 tropical
Australian estuaries. Marine Ecology Progress Series,
385: 245-260. doi: 10.3354/meps08040
Sheaves, M., Johnston, R. & Abrantes, K. 2007. Fish
fauna of dry tropical and subtropical estuarine
floodplain wetlands. Marine and Freshwater Research,
58: 931-943. doi: 10.1071/MF06246
Sheaves, M., Johnston, R. & Conolly, R.M. 2012. Fish
assemblages as indicators of estuary ecosystem health.
Wetlands Ecology and Management, 20: 477-490. doi:
10.1007 /s11273-012-9270-6
Shoji, J., Masuda, R., Yamashita, Y. & Tanaka, M. 2005.
Effect of low dissolved oxygen concentrations on
behavior and predation rates on red sea bream Pagrus
major larvae by the jellyfish Aurelia aurita and by
juvenile Spanish mackerel Scomberomorus niphonius.
Marine Biology, 147(4): 863-868. doi: 10.1007/
s00227-005-1579-8
Sindilariu, P., Freyhof, J. & Wolter, C. 2006. Habitat use
of juvenile fish in the lower Danube and the Danube
delta: implications for ecotone connectivity.
Hydrobiologia, 571: 51-61. doi: 10.1007/s10750-006-
0216-y
Stein III, W., Smith, P.W. & Smith, G. 2014. The cast net:
an overlooked sampling gear. Marine and Coastal
Fisheries, 6: 12-19. doi: 10.1080/19425120.2013.864
737
Stewart, A.J.A., John, E.A. & Hutchings, M.J. 2000. The
world is heterogeneous: ecological consequences of
living in a patchy environment. In: Hutchings, M.J.,
John, E.A. & Stewart, A.J.A. (Eds.). The ecological
consequences of environmental heterogeneity.
Blackwell Science, Oxford, pp. 1-8.
Sundblad, G. & Bergström, U. 2014. Shoreline develop-
ment and degradation of coastal fish reproduction
habitats. Ambio, 43(8): 1020-1028. doi: 10.1007/
s13280-014-0522-y
Tecchio, S., Rius, A.T., Dauvin, J.C., Lobry, J., Lasalle,
G., Morin, J., Bacq, N., Cachera, M., Chaalali, A.,
Villanueva, M.C. & Niquil, N. 2015. The mosaic of
habitats of the Seine estuary: insights from food-web
modelling and network analysis. Ecological
Modelling, 312: 91-101. doi: 10.1016/j.ecolmodel.
2015.05.026
Velázquez-Velázquez, E., Vega-Cendejas, M.E. &
Navarro-Alberto, J. 2008. Spatial and temporal
variation of fish assemblages in a coastal lagoon of the
Biosphere Reserve La Encrucijada, Chiapas, Mexico.
Revista de Biología Tropical, 56(2): 557-574. doi:
10.15517/RBT.V56I2.5608
 Fish assemblages in a shallow lagoon-estuarine system
Verdiell-Cubedo, D., Torralva, M., Ruiz-Navarro, A. &
Oliva-Paterna, F.J. 2013. Fish assemblages in different
littoral habitat types of a hypersaline coastal lagoon
(Mar Menor, Mediterranean Sea). Italian Journal of
Zoology, 80: 104-116. doi: 10.1080/ 11250003.2012.
686525
Warburton, K. 1978. Community structure, abundance
and diversity of fish in a Mexican coastal lagoon
system. Estuarine, Coastal and Shelf Science, 7(6):
497-519. doi: 10.1016/0302-3524(78)90061-0
Webster, I.T. 2011. Dynamic assessment of oceanic
connectivity in a coastal lagoon-the Coorong,
Australia. Journal of Coastal Research, 27(1): 131-
139. doi: 10.2112/JCOASTRES-D-10-00079.1
Whitfield, A.K. 1998. Biology and ecology of fishes in
South African estuaries. Ichthyological Monographs 2.
J.L.B. Smith Institute of Ichthyology, Grahamstown,
223 pp.
Received: 23 April 2019; Accepted: 5 July 2019
37
Wilkinson, T., Wiken, E., Bezaury-Creel, J., Hourigan, T.,
Agardy, T., Herrmann, H., Janishevsky, L., Madden,
C., Morgan, L. & Padilla, M. 2009. Marine ecoregions
of North America. Commission of Environmental
Cooperation, Montreal, 177 pp.
Yáñez-Arancibia, A., Lara-Domínguez, A.L., Chavance,
P. & Flores-Hernández, D. 1983. Environmental
behavior of Términos Lagoon ecological system,
Campeche, Mexico. Anales del Instituto de Ciencias
del Mar y Limnología, 10(1): 137-176.
Yáñez-Arancibia, A., Lara-Domínguez, A.L., Sánchez-
Gil, P. & Day, J.W. 2004. Interacciones ecológicas
estuario-mar: marco conceptual para el manejo
ambiental costero. In: Caso, M., Pisanty, I. & Ezcurra,
E. (Eds.). Diagnóstico ambiental del Golfo de México.
Secretaría del Medio Ambiente y Recursos Naturales,
Instituto Nacional de Ecología, México D.F., pp. 431-
490.
Zar, J.H. 2010. Biostatistical analysis. Prentice-Hall, New
Jersey.